The Animal Mind: A Textbook of Comparative Psychology

Harper (289) in 1911 revived the mechanical theory of the geotropism of Paramecium. He argued that an animal which, like this protozoén, moved in a spiral could hardly use the changes of position of internal particles as effective stimuli. The reaction of Paramecium can be altered by altering the specific gravity of its body, as by causing it to absorb particles of iron or paraffin. When it has ingested iron, its responses are modified by the neighborhood of a

magnet (290). Wager (751) maintains that geotropism in Euglena also is purely passive, due to the fact that the hinder end of the animal is the heavier. Kanda (389) has recently championed the “‘statocyst”’ theory of Lyon, as against the mechanical theory, using Lyon’s argument that when Paramecia are rapidly rotated i in an apparatus called a “centrifuge,” their front ends are directed outward by centrifugal force and therefore must be heavier, instead of lighter, as the mechanical theory would require. Harper had previously attempted to meet this objection by regarding such a position on the part of the centrifuged animals as due not to centrifugal force but to compensatory movements made actively by the animal. Both the mechanical theory and the “‘statocyst” theory, then, seem to be still on the field.

It has been shown that the reactions of Paramecium to gravity are modified by a variety of conditions. Negative geotropism, in a sense its normal condition, is favored by plentiful food supply and by an increase in temperature within certain limits ; positive geotropism, movement downward, may be brought about temporarily by mechanical shock, by salts and alkalies, by temperature changes (503, 689), to which, however, the animals may adapt themselves ; with less constancy by increase in the density of the fluid containing them, and with lasting effect by lack of food. It has been suggested that the downward movement under these circumstances is protective, since it shields the animals from surface agitation of the water, from surface ice, and from failure of the surface food supply (500). We shall see that similar conditions often change the direction of an animal’s response to light.

Among the ccelenterates, geotropism is shown by certain hydroids, whose stems have a tendency to curve upward and their ‘‘roots” a tendency to grow vertically downward when the animals are placed in a horizontal position (714). The sea-anemone Cerianthus, whose normal position is head upward, will right itself if placed in any other position, though the righting reaction may be inhibited by contact stimulation on the side of the animal. It ordinarily lives with the body enclosed in a tube, and when taken from its proper habitat it seems to “prefer” a position, even horizontal, where the sides of the body are in contact with a solid, to a vertical position with its sides uncovered (424). The righting reaction of Hydra is not determined by gravity at all; the animal will take any position, vertical or horizontal, but “seeks” always to have its foot in contact with a solid (751 a). Some actinians have shown an interesting modification of gravity reaction through what we may call habit. Six specimens of Actinia equina were selected that had been fixed to the rocks in an ‘“‘upside-down”’ position, that is, with the mouth end downward; and six others that had been right side up. In the first experiment all were placed upside down; the tendency to right themselves was decidedly stronger in those which had been previously erect. Similarly, when twelve selected in the same way were all placed right side up, the ones that had previously been in the reversed position showed a certain inclination to reassume it (258). On the other hand, the orientation of the polyp Corymorpha palma to gravity was entirely unaffected by keeping the animal for a long time in a position where it could not right itself; it assumed the upright position as soon as it was set free (714).

It was noted in the chapter on hearing that the peculiar organs occurring in certain Coelenterata and in many other animals, which were originally called otocysts because of their supposed auditory function, have had their name changed to that of statocyst since it has appeared that they subserve chiefly orientation to gravity. In jellyfish, removal of these organs does not seem to affect the animal’s power of keeping its balance; apparently equilibrium is maintained here by the simple action of gravity, for dead jellyfish float in the right-side-up position (514, 521). It has been suggested that the statocyst organs are for the reception of stimuli produced by shaking, to which meduse are apparently sensitive (521). Negative geotropism exists in Gonionemus, which swims to the surface of the water when disturbed (825). In ctenophors, the statocyst organ, which is usually at one pole of the body, has been found to function as an organ for the maintenance of equilibrium

A good example of a specially developed reaction having for its result the “‘righting” of an animal in an abnormal position is offered by the behavior of a planarian that has been turned over so that its back rests on the surface of support. The reaction consists of a turning of the body, beginning with the head end, about the long axis, so that a spiral form is assumed. The dorsal surface of the animal is convex, the greatest thickness of the body being in the middle line. When the planarian lies on its back, it thus naturally tips to one side, like a keeled boat out of water. This side, being brought into contact with a solid, gives a reaction analogous to the negative one, that is, it extends or stretches. Such a stretching of one side when the

planarian is right side up would of course produce a turning in the opposite direction, a negative reaction. In this case, however, the opposite side does not contract to allow of turning, but maintains the same length. The necessary result is that the body is thrown into a spiral: as soon as the ventral surface of the head comes into contact with the solid, in consequence of the turning, the negative reaction of that end ceases. Thus the righting is progressively accomplished (561). The whole response can hardly be classed under the head of geotropism. Like that of Hydra, it is not made as the result of the pull of gravity, but is a reaction to contact stimulation; the animal will crawl in an upside-down position as readily as any other provided that the ventral surface and not the dorsal is in contact with a support.

Geotropism, in the marine worm Convoluta roscoffensis, has been found to fluctuate with the rise and fall of the tides, even when the animal is removed to an aquarium. In normal life the worms burrow in the sands at rising water, and come to the surface when the tide retreats. Prolonged exposure to air, or increase in the intensity of the light, causes them to move down the slope of the shore to moist places. These movements in the normal environment are represented by upward and downward movements of the animal when confined in a glass tube. Keeble and Gamble thought these oscillations in geotropism did not occur in darkness, and that the stimulus bringing them about was photic. When the summation of light stimuli passes a certain amount, they maintained, positive geotropism appears ; when the after effect of light stimulation is dissipated, the

negative phase recurs (253). Bohn, however, finds that the oscillations do persist in darkness, and that their primary cause is the mechanical shock of the waves, as is further indicated by the observation that shaking the tube will cause the worms to descend (61). The geotropism of Convoluta is dependent on the statocyst (253). Among Mollusks, the slug has had its reactions to gravity carefully observed. When placed in a horizontal position on an inclined glass plate, these animals tend to turn either upward or downward, moving either with or against the force of gravity. Davenport and Perkins found that the same individuals differed at different times in this respect, and concluded that the sense of the geotropism was determined by obscure conditions. They also found that an inclination of only 7.5° on the part of the glass plate, representing only 13° of the full force of gravity, is sufficient to make the slugs orient themselves with reference to the pull of the earth, though the precision of such orientation increases as the angle increases (175). Frandsen thought it was the weight of the posterior part of the body that determined whether the movement should be up or down: that the natural tendency of all was to go downward, but that in some individuals the posterior part, which is poorly controlled, was heavier than the anterior, and pulled the animal around head upward (236).

Kanda (392, 393), on the other hand, thinks flint in freshwater and marine snails the statoliths are the organs determining orientation to gravity, and that it is not merely passive: he claims to have observed that this orientation is most marked, the less the slope of the surface on which the animal crawls. The response of Physa, a freshwater snail, to gravity depends in an interesting way on the animal’s physiological condition: when the snail is in need of air it is strongly negative in its geotropism, ‘crawling upward towards the surface of the water and disregarding all other stimuli: as soon as its lungs are full of air it is no longer sensitive to gravity (177). Buddenbrock (107, 108, 109) and Baunacke (29-32) have brought evidence to support the view that the statocysts in many mollusks are useful not so much in securing orientation to gravity, which is of little importance in such slow-moving animals, but rather in enabling them to right themselves, to direct their movements, and to dig in the sand. The statocyst organs in a cephalopod, Eledone, have been shown to function in maintaining equilibrium (249).

Righting reactions in the starfish have been described by Romanes (641). The tips of two or three rays are twisted around until the suckers in the ventral side have a firm hold of the supporting surface; the twisting is then continued, always in the same direction on the different rays, until the whole body is turned. Jennings (380) enumerates twelve different factors which determine which particular rays shaJl twist over and attach themselves first, but Moore (501) thinks that the ‘‘positive stereotropism,”’ that is, the tendency to remain in contact with solids, of the tube feet is a sufficient explanation. It is not clear how a tendency to remain in contact with a mechanical stimulus can explain a tendency to seek such a stimulus when it is absent, and Jennings’s view, that the original impulse to turn comes from the general state of unrest in which the

animal is thrown by its position, seems plausible. But what is the stimulus inducing the unrest? Not contact of the back with a solid object, for a starfish is not disturbed if its back is touched when it is crawling in the ordinary position; and not merely having its back. directed downward, for it will crawl upside down on the under surface of rocks. Something abnormal about the stimulation of the tube feet when they are in contact, not with a solid support, but with the water flowing over them, must present the condition for the internal state of instability which occasions the twisting movements of the rays.

The sea-urchin, ‘‘a rigid, non-muscular, and globular mass,”’ as Romanes calls it, with relatively feeble suckers, has a much harder time to right itself, and does not succeed in pulling itself over unless it is perfectly fresh and vigorous. It occasionally rests for some time when it has reached a position of stability halfway over, before continuing the process (641). Lyon has observed marked negative geotropism in the larve of the sea urchin. He was unable to test Davenport’s theory of the nature of the geotropic response by putting the animals in a solution of the same density as their own bodies, for the reason that such a fluid was too dense and sticky (being made of gum arabic and sea water) for them to swim in. That the response was merely a passive one he thinks improbable, because the larve from eggs that have been rapidly rotated, or “‘centrifuged,’’ as it is called, have all the pigment on one side of their bodies and may therefore be supposed to have their ordinary balance disturbed; yet they rise to the surface just like the rest (450).

That the statocyst organs in Crustacea are probably connected with equilibrium rather than with hearing we have already seen. Delage in 1887 found that Mysis, Palemon, and other forms displayed serious disturbance of equilibrium when both eyes and statocysts were destroyed, showing that the eyes also play a part in the maintaining of balance (180). The eyes have been found to codperate with the statocysts in the fiddler crab, Gelasimus, and also in another decapod, Platyonichus (127). Neither of these has statoliths. Peneus membraneus, on the other hand, was found to be permanently disoriented by destruction of the statocysts or even removal of the statoliths, while blinding produced no great disturbance, probably because of the animal’s nocturnal habits (38, 250). Young crayfish with the statocysts destroyed will swim upside down as readily as right side up (111). But the prettiest evidence for the static function of the statocysts was obtained when powdered iron was substituted for the mineral bodies in the open statocysts of Palemon. It was found that when a magnet was brought near, the animal would respond by taking up a position corresponding to the resultant of the pull of the magnet and that of gravity (407).

Specific righting reactions occur in many Crustacea, though in some cases these seem to be merely the incidental effects of ordinary locomotion. Branchipus, the fairy shrimp, normally swims upside down; if turned right side up when moving along the bottom of the vessel, it continues to move in this position without showing any disturbance until it happens to rise a little from the bottom, when apparently the weight of the body pulls it around into the usual upside-down position. The crayfish has two methods

of righting itself: a quick “flop” executed with the tail, and a slow and laborious raising of itself on one side and tipping over (179). Many Crustacea show marked responses to gravity: for example, Parker found decided negative geotropism in the females of the marine copepods whose depth migrations he studied. It seems to be needed to counteract the tendency of the animals to fall to the bottom by their own weight (534). In certain copepods, light was observed to change the sense of the response to gravity, not by taking its place as a directive stimulus, but apparently by producing some physiological change in the animals. Their normal geotropism was positive, that is, they had a tendency to move downwards. In darkness, however, their geotropism became negative. They were also negatively phototropic to strong light. If, when in the negatively geotropic phase, they were illuminated from below by intense light, from which they would ordinarily have moved away, the change from negative to positive geotropism induced by the light was of sufficient influence to make them move downward toward it (210). Other facts regarding the relation of geotropism and phototropism are mentioned on pp. 209 ff.

Spiders and insects have no statolith organs. Bethe thinks that equilibrium is maintained in their case as a natural result of the position of the centre of gravity and the distribution of air in the body. He supports this view by experiments in which dead insects, allowed to fall through the air, assume the normal position, and is inclined to think that all animals without special static organs maintain their balance in this way (48). Negative geotropism in certain

insects, as evidenced by a tendency to creep from horizontal planes up vertical ones, was observed by Loeb (420). In light the eyes of insects have probably much to do with maintaining equilibrium. Certain aquatic insects, in experiments where the light was made to strike them only from below, as soon as they left the support on which they were resting, turned themselves upside down (622). It has long been known that in vertebrates the static function resides in the ear, and especially in the semicircular canals (e.g. 103, 165, 229, 263). Various experimenters have noted that operations on the ears of fishes disturb the equilibrium of these animals. Sewall, indeed, found that section of the semicircular canals in the shark had no effect on its balancing powers, although operations on the vestibule and ampulle did disturb movement (669); and Steiner got no effect on equilibrium from removing the contents of the labyrinth (692). Errors in method and observation probably influenced these results. Loeb found that severing the auditory nerve or removing the statolith from the dogfish caused the fish to incline toward the operated side and to roll the eyes in that direction (424). Total extirpation of one labyrinth in the perch was observed by Bethe to make the fish curve toward the affected side. The fish Scardinius showed a tendency to curve toward the opposite side (48). Lee’s experiments on the dogfish showed a very definite relation between the position of the canal operated upon and rolling movements of the fish. Cutting the front canals caused the fish to dive forward, cutting the rear canals made it dive backward, and cutting the canal on either side made it roll over toward that side. A natural

explanation of this behavior is to suppose that the absence of stimulus from the cut canal produces the same effect that rolling the fish in the opposite direction, and thus diminishing the pressure of the fluid in the canal, would produce. The fish “‘feels as if” it were being rolled over, and makes movements: to regain its equilibrium. When the nerves supplying the ears on both sides were cut, the fish became perfectly indifferent to its position and would float upside down without any effort to right itself. The vestibule and otoliths of the fish ear are thought by Lee to be concerned with static equilibrium; that is, with the maintenance of position while the fish is at rest, while the canals are concerned with balance during motion (dynamic equilibrium) (416). It may be added that experiments on the sea horse indicate that destruction of the labyrinths in this animal has no effect on equilibrium: the upright attitude is due to the position of the air bladder and is assumed even by dead animals (251).

That vision may materially aid in maintaining equilibrium in vertebrates is indicated by evidence from various sources, among others, the observation of Bigelow that goldfish in which the nerves supplying both ears had been cut recovered after two or three weeks and could swim quite normally except when they were placed in a large body of water and made to swim rapidly, when they showed no power of preserving their balance (54). Their successful performance of slower movements was very likely due to the use of sight.

Sensory impulses from the body muscles themselves undoubtedly codperate with those from the semicircular canals in the maintenance of balance. They are evidently involved in the peculiar withdrawing movements by which land animals, even puppies, kittens, and young rats whose eyes have not opened, save themselves from falling when they reach the edge of the object on which they have been crawling (490, 683). Water-dwelling animals, accustomed to plunge off solid supports, lack this protective instinct ; Yerkes showed that among several species of tortoises, some land-dwelling, some amphibious, and some aquatic, the first mentioned were much more reluctant than the second to crawl off the edge of a board, and the second more reluctant than the third (810).

Glancing back over these examples of the responses made by animals to gravity, we note that while in some cases the earth’s attraction appears to act mechanically upon the animal, causing the body passively to assume a certain position, the common method of bringing about orientation seems to be that some structure in the body,,placed in an abnormal position, presents a stimulus which brings about ‘acompensatory movement. This structure may be heavier particles of the body substance, as probably is the case in Paramecium ; it may be a statolith, or the fluid in the labyrinth; it may be the eyes. In any case, what shall we say about the sensation quality involved? Perhaps the reactions produced are wholly reflex. Perhaps the statolith or the canal fluid produces a specific sensation quality. Or perhaps, as Verworn thinks, the sensation quality is merely that of pressure (741). Whatever its nature, spatial perception, the perception of the spatial relations between several stimuli simultaneously apprehended, plays no part in the orientation of animals to gravity.

In some animals light is sought or avoided not simply because of the fact that in certain intensities it stimulates to restlessness and activity (photokinesis), so that they come to rest in regions illuminated by other intensities ; but through a direct movement of the animal towdrds or away from the source of light. It is this type of response to which Loeb and his followers restrict the term “‘tropism.”’ Plants show it, both in the orienting of their stems with relation to light, and in the movements of their freely swimming “swarm spores.” In the case of animals, it is illustrated by the behavior of the sea-anemone Actinia cereus. Weak light causes expansion of the tentacles of this organism perpendicularly to the light rays. If the light is increased, Bohn (86) says the tentacles ‘‘tend to orient themselves in the direction of the rays, and finally converge in a bundle parallel to that direction,’”’ a response which has the effect of protecting them from the intense light. Again, the tubedwelling worm Spirographis spallanzanii. gradually curves its tube until its mouth end faces the direction from which the rays of light come, and another marine worm, whose tube is absolutely stiff, adapts itself to a change in the direction of the rays by curving the newly formed portions of the tube as it constructs them (422).! Sea-anemones and tube-dwelling worms closely resemble plants in their mode of living. In freely moving animals, where the oriented movement is made in response to light, it is commonly preceded by body orientation; that is, the body first faces or turns tail to the light, and the animal then moves forward. Sometimes, however, there is no regular body

1 Hargitt (288) finds no such constancy of orientation in Spirographis as orientation; the animal moves, for instance, always away from the light, which means that it moves forward if its body happens to be oriented with the tail to the light, or backward if its head happens to be directed to the light. Such behavior is reported by Holmes of mosquito larve (338) and by Gee of leeches (257). On the other hand, Hadley (274) says that young lobsters always orient with the head towards the light, though they may move either away from or towards it. In some animals with eyes, such as the crustacean Daphnia, there is reason to think that body orientation is primarily an affair of eye-orientation or fixation. This at least is the view of Radl (621). He placed Daphnia under a microscope in such a way that only the eyes could be moved. When the light coming from below was diminished, the eyes rolled upward; when the light coming from above was diminished, the eyes rolled downward. Holmes (330) observed that in amphipods, blackening one eye of a positively phototropic animal causes a turning toward the blackened side, as if the animal were trying to restore the missing illumination; similar experiments upon negative animals produced turning towards the other side.

It is the view of Loeb (434). that oriented response of animals to light is wholly analogous to the same type of response in plants. Since plants with their very slow and limited movements are subject more to light as a continuous - stimulus than to sudden changes in light intensity, orientation in their case must be brought about by the steady and continuous action of the light. Accordingly, Loeb maintains the view that the tropism or oriented response of animals to light is dependent on the continuous action’ of the light, and not on changes in light intensity. It is thus a mode of response that has nothing in common with “‘sen-

sibility to difference,” which Loeb recognizes as an independent form of reaction. In support of his continuous action theory Loeb lays great stress on the proof, by the botanist Blauuw, that the ‘‘Bunsen-Roscoe Law,” that is, the law that the effect of weak light acting a long time is equal to that of strong light acting a short time, holds for plants; Loeb thinks it holds also for animals. The action of continuous light in producing a tropism has been explained in two ways: (1) as the effect of the direction of the light rays traversing the animal’s body, and (2) as the effect of having symmetrical points on the animal’s body stimulated with unequal degrees of intensity. In his earliest discussion of the subject, Loeb (419) expressed himself positively in favor of the former hypothesis. ‘The orientation of animals to a source of light is, like that of plants, conditioned by the direction in which the light rays traverse the animal tissue, and not by the difference in the light intensity on the different sides of the animal.’’ Bohn, in general the ardent follower of Loeb, urged as a ‘“‘fundamental objection”’ to this that “the ‘luminous rays’ which strike a living body have, save in wholly exceptional cases, various directions, being reflected, diffused, and refracted by neighboring bodies”. (80). Moreover, the animal bodies which are opaque could not be traversed by light rays. Loeb seems later to have abandoned the “‘direction theory” of the tropism. The ‘intensity theory” was first proposed by Verworn (743).

How can differences in the intensity of a stimulus falling ‘upon symmetrical and opposite points on an animal’s body bring about orientation? Let us call the two points a and a’, a being a point on the right side of the animal’s body and a’ a symmetrically placed point on the left side. Suppose the animal has a tendency to orient itself positively to the light, that is, turn towards the light, and suppose a ray of light strikes it obliquely from the right. Evidently the point a receives a greater intensity of the stimulus than the point a’. Now if the animal is positive to light, Loeb would suppose that its chemical constitution is such that light causes, either by direct action on the muscles or reflexly through the eyes, a contraction of the muscles. Hence the muscles at point a, or controlled through point a, would contract more strongly than those at point a’: the animal in consequence would turn towards the right, that is, towards the light, and would continue so turning until the light struck a and a’ with equal intensity, that is, until it directly faced the light. All subsequent movement would have to be directed straight towards the light. If the animal is negative in its response to light, then it is so chemically constituted that light causes a relaxation of the muscles. In such a case, the point least strongly stimulated would produce the strongest muscular contractions: the animal would turn towards that side, and would continue turning until opposite points were equally stimulated, that is, until it headed directly away from the light: all subsequent movement would have to be in this direction.

Now Jennings (373), has suggested that the oriented reactions of certain organisms, at least, are really due to changes in the intensity of the light, brought about by the animal’s own movements. This view would, if generalized, put all directed light reactions in the ‘‘sensibility to difference” class given to changes in intensity: the effect of continuous light would be limited to photokinesis. Let us see how an oriented response may be conceived to result from reactions to changes in light intensity. In the Protozoa, according to Jennings (373) and Mast (463), the orientation is

due to negative reactions given when the organism in its ordinary swimming movements, which usually involve turning from side to side, either passes into a region of greater or less illumination, or swings its anterior end ‘toward or away from the source of light, so that it is shaded at one moment and strongly illuminated at the next.” Suppose, that is, an animal makes in its locomotion slight random movements of the head from side to side. Suppose that one side of it is more brightly illuminated than the other. If the animal is positive to light, it has the characteristic of making a negative response whenever its head end is suddenly darkened. This will happen when the head end is accidentally turned away from the light; consequently all such random movements will be checked, while random movements of the head towards the light will not be checked. Hence the animal will turn until its head points towards the light: in this position random movements towards either side will be equally checked because they will equally tend to bring the head into a darker region; and so movement will take place in a line generally towards the light, though still with balanced random movements to either side. If the animal is negative, it has the characteristic of making negative reactions when the illumination of the head is suddenly increased, and obviously this will bring about orientation with the head end away from the light.

In Volvox (see page 136), orientation is held by Oltmanns (528) and Mast (464) to occur after this fashion. The reaction of a Volvox colony, which in moderate light is positively phototropic, takes place in consequence of a response by each individual in the colony given when, as the colony rotates, that individual passes from a higher to a lower intensity of light. A point which has been regarded as of much importance in deciding between the theories of Loeb and Jennings on orientation to light is the actual occurrence or non-occurrence of random movements. Thus Holmes (334) believes the negative orientation of earthworms to light occurs by the checking of random movements of the head towards the light. In the crawling movements stimulated when light is thrown upon the worm, the head is turned from side to side. If it happens to be turned toward the light, it is withdrawn. Holmes explains the observation of Parker and Arkin that the head of the worm is much more apt to turn from the light than toward it (552), by saying that account was probably taken here only of the first decided turn made. He himself experimented by lowering a worm, crawling on a wet board, while its body was in a straight line and contracted, into a beam of light at right angles to the body, and noting the first movement of the head. This was found to be twenty-seven times away from the light and twenty-three times toward the light. A similar method of orientation by “trial and error” was observed in the leech and in fly larve by Holmes (334).